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Acta zoologica cracoviensia, 46(suppl.– ): 25-36, Kraków, 15 Oct., 2003

Palaeoentomology: towards the big picture

Edmund A. JARZEMBOWSKI

Received: 1 Feb., 2002 Accepted for publication: 1 June, 2002

JARZEMBOWSKI E. A. 2003. Palaeoentomology: towards the big picture. Acta zoologica cracoviensia, 46(suppl.– Fossil Insects): 25-36. Abstract. Insects (Superclass ) are the most palaeodiverse as well as the most biodiverse organisms of all time but probably total under 20 million species. Familial/ge- neric data agree with an exponential growth model of the of terrestrial . Ordi- nal data is consistent with a logistic model but with a major perturbation superimposed (the ). The global taxonomic carrying capacity is about 31 for orders whereas familial and species data suggest power functions. Key events in the record are briefly discussed. Key words: insects, , palaeodiversity, , evolutionary patterns. E. A. JARZEMBOWSKI, Maidstone Museum & Bentlif Art Gallery, St Faith’s St., Maid- stone, Kent, ME14 1LH and P.R.I.S., Reading University, UK. E-mail: [email protected]

I. BIODIVERSITY AND PALAEODIVERSITY

Insects comprise well over 50 percent of global species biodiversity (Figs 1, 2). The description of new insect species is more or less exponential (Fig. 3). In contrast, the recognition of new insect orders is in decline (Fig. 4: total). The description of new insect orders peaked in the nineteenth cen- tury. This was mainly due to the impact of various living orders being erected (Fig. 4: extant). It re- mains possible, however, that more fossil orders will be recognised in the future (Fig. 4: extinct). Some workers maintain that evolutionary change is best studied at the species level (WILLMANN 1997) but others consider that databases are a good proxy (BENTON et al. 2000). At family level, insects are the most diverse group in the fossil record (BENTON 1993: fig. P.2). Trend lines based on family palaeodiversity suggest that insects total under 20 million species (JARZEMBOWSKI &ROSS 1993: Fig. 9; this paper, Fig. 10). This agrees with the current tendency by entomologists to estimate a total of less than the 50 or even 100 million species proposed during the heyday of Erwin- ian estimates. Acknowledgements.Iwish to thank Prof. M. BENTON (Bristol University) and Mr R. CORAM (Reading University) for some copies of papers consulted and Drs A. GOROK- HOV (Zoological Institute, Russian Academy of Sciences), W. KRZEMIÑSKI (Natural History Mu- seum, Polish Academy of Sciences), C. LABANDEIRA (Dept. of , National Museum of Natural History, Smithsonian Institution), A. NEL ( Laboratory, National Museum of Natural History, Paris) and D. SHCHERBAKOV ( Laboratory, Palaeontological Institute, Russian Academy of Sciences) for comments towards Fig. 10. This is P.R.I.S. contribution. E. A. JARZEMBOWSKI 26

Fig. 1. Global biodiversity based on known species (approximately 1.454 million). After CRANBROOK (1996), WILSON (1992).

Fig. 2. Estimated global biodiversity (approximately 65.654 million). Based on references in Fig. 1.

Fig. 3. Rate of description of insect species. After BENTON (2001). Palaeoentomology: towards the big picture 27 Table I Time ranges of insect orders

1. SILVESTRI, 1907* – R 2. Collembola LUBBOCK, 1871* D1-R 3. BÖRNER, 1904* two-pronged bristletails C2-R 4. BÖRNER, 1904* bristletails D2?-R 5. SHAROV, 1951* – C2-P 6. BÖRNER, 1904* C2-R GOLDENBERG, 1877* 7. – C2-P2 + Permothemistida SINITSHENKOVA, 1980. 8. BRONGNIART, 1885* – C2-P 9. HANDLIRSCH, 1919* – C2-P 10. Ephemeroptera HYATT &ARMS, 1890* C2-R 11. Protodonata BRONGNIART, 1893* ‘giant ’ C2-Tr3 12. FABRICIUS, 1793* dragonflies C2-R 13. ‘’ HANDLIRSCH, 1906 – C1-Tr 14. BURMEISTER, 1838* stoneflies P1-R 15. SHIPLEY, 1904* web-spinners P1-R 16. BRUNNER, 1893* stick insects P2-R 17a. OLIVIER, 1789* crickets, grasshoppers, locusts C2-R 17b. SHAROV, 1968 – Tr 18. Grylloblattodea BRUES &MELANDER, 1915* – P1-R 19. TILLYARD, 1931 – P 20. Dermaptera DE GEER, 1773* J1-R 21. MARTYNOV, 1927* – C2-J1 22. BRUNNER, 1882* C2-R 23. Isoptera BRULLÉ, 1832* K1-R 24. Mantodea BURMEISTER, 1838* praying K1-R 25. Caloneurodea HANDLIRSCH, 1937 – C2-P 26. SILVESTRI, 1913* – O-R 27. SHIPLEY, 1904* booklice P1-R 28. Phthiraptera HAECKEL, 1896* lice E-R 29. Thysanoptera HALIDAY, 1836* P1-R 30. LINNÉ, 1758* bugs C2-R 31. MARTYNOV, 1938 – P1-J3 32. KIRBY, 1815* stylopids E-R 33. Coleoptera LINNÉ, 1758* P1-R 34. Raphidioptera LATREILLE, 1810* P2-R 35. LATREILLE, 1802* alder flies P1-R 36. LINNÉ, 1758* lacewings P1-R 37. LINNÉ, 1758* , ants, bees Tr3-R 38. Trichoptera KIRBY, 1815* P1-R 39. LINNÉ, 1758* , butterflies J1-R 40. Diptera LINNÉ, 1758* flies Tr2-R 41. Siphonaptera LATREILLE, 1825* K1-R 42. PACKARD, 1886* scorpionflies P1-R

Key: D1, Lower , ca 398 Ma; D2, Middle Devonian, ca 391 Ma; C1, Lower ; C2, Upper Carboniferous, ca 307 Ma; P, ; P1, Lower Permian, ca 251 Ma; P2, Upper Permian, ca 273 Ma; Tr, Triassic; Tr3, Upper Triassic, ca 222 Ma; J1 Lower , ca 193 Ma; J3, Upper Jurassic, ca 151 Ma; K1, Lower , ca 121 Ma; E, Eocene, ca 46 Ma; O, Oligocene, ca 29 Ma; R, Recent, 0.01 Ma-.

* (DUNCAN, 1997 and references therein) E. A. JARZEMBOWSKI 28

No. of Orders

20 18 Total

15 16 15

Extant

10 9 8

5 Extinct 3

0

18th 19th 20th Century

Fig. 4. Rate of description of insect orders: extinct (dotted line), extant (solid) and total (dotted-and-dashed). Data from Table I.

II. PHANEROZOIC PATTERNS

BENTON &HARPER (2000) suggested that there is a difference in style between evolution in land organisms as compared with evolution in the marine realm. They considered that terrestrial life has evolved exponentially whereas life in the sea has evolved logistically (cf. Fig. 5). Insects are crucial to this discussion because they are a significant element of terrestrial life (JARZEMBOWSKI 2001). Generic and familial data suggest exponential growth during the Phanerozoic (Figs 6, 7). In con- trast, ordinal data suggest a logistic (sigmoidal) pattern but with a major perturbation superimposed – the Triassic extinction (Fig. 8). If the effect of the latter is subtracted, then ordinal diversity levels off at about 31 orders from a total of about 42 orders of insects. BENTON (2001) considered that, in general, a logistic pattern at high taxonomic level could de- cay into an exponential pattern at low taxonomic level. He based this on HOLMAN’s (1996) statisti- cal analysis which concluded that /family/ curves of diversity could be real (genetic) or an artefact (taxonomic). KERR (2001) has, however, doubted some of BENTON’s data source. HOLMAN (op. cit.) suggested that a real signal could be obtained by the use of monophyletic groups (as in ) and supporting morphological data although GRANTHAM (2001) considered that some paraphyletic taxa are real. In this connection it may be noted that the great majority (90%) of insect orders used in Fig. 8 are considered to be monophyletic (Table I). In addition, mouthpart data for insects shows a logistic pattern (Fig. 9) providing supporting morphological data. This is, however, not easily reconciled with a phyletic approach to palaeodiversity (ALEKSEEV et al. 2001). The testing of congruence between phylogeny and the fossil record is at an early stage (WILLS 2001). Interestingly, Atelocerata ( + Hexapoda) is more congruent than an (Insecta + Crustacea) advocated more recently (DEUVE 2001). Palaeoentomology: towards the big picture 29

Fig. 5. Ideal curves for exponential (unlimited) and logistic (sigmoidal/constrained) growth.

Fig. 6. Cumulative curve for insect generic diversity from Devonian to Recent. Points are totals by period (black circles) and subperiod (open circles). Abbreviations: Pl – Pliocene; M – Miocene; O – Oligocene; E – Eocene; P – Palaeocene; K – Cretaceous; J – Jurassic; Tr – Triassic; P – Permian; C – Carboniferous; D – Devonian; 1, 2, 3, Lower, Middle, Upper. No.s, Ma. Data in JARZEMBOWSKI &ROSS (1996). E. A. JARZEMBOWSKI 30

Fig. 7. Cumulative curve for insect family diversity. Explanation as in Fig. 6 except points joined by dashed line.

III. HYPERDIVERSITY

According to HOLMAN (1996) non-insectan higher taxa include an average of 6-12 lower taxa. In contrast, insect orders contain an average of 30-40 families. The 32 extant orders of insects total 967 families (NAUMANN 1995). Families are therefore the number of insect orders nearly to the power two (322 = 1,024). The 42 extant plus extinct orders (including the unnatural order Protor- thoptera) contain over 1,275 families (ROSS et al. 2000). Nearly 70 percent of extant families are known as fossils (JARZEMBOWSKI 2001a) suggesting that at least another 290 families remain to be found. This would give a total of 1,565 families for the Phanerozoic, or nearly the total of natural orders to the power two (412 = 1,681). Interestingly, insect orders to the power four is 2.8 million, approximately the lower estimate of insect species biodiversity (some 3 million species; BENTON 2001). Insects may be justifiably referred to as hyperdiverse (MAY 1995)! If the effect of the Trias- sic extinction is ignored by extrapolating from the Permian to Recent, then Phanerozoic ordinal di- versity could level off at about 31 orders (Fig. 8). This is close to the number of extant insect orders (32) and, curiously, the number of phyla (31, NIELSEN 1995). Palaeoentomology: towards the big picture 31

Fig. 8. Cumulative curve for insect orders. Permian – Recent extrapolation, dashed line; ‘K’ value, dotted line. Roman nu- merals indicate key events (see text). Orders in Tab. I. Other explanation as in Figs 6, 7.

IV. KEY EVENTS

These are indicated by roman numerals in Fig. 8 and summarised below: I – earliest hexapods (insects senso lato); II – earliest true insects (Zygentoma + ); earliest flying insects (Pterygota); III – near-modern range of plant-feeding strategies in insects; IV – radiation of insects with complete (Holometabola); V – earliest insectan parasites (Diptera); VI – earliest amberized insects; earliest definite social insects (Isoptera). Comments:thehexapod radiation beginning in the Carboniferous seems to have been an adaptive one as opposed to mere contingency because it entailed significant (Table I, Fig. 10). The Carboniferous radiation of the pterygotes effected Paleoptera and , whereas the Permian one effected and Oligoneoptera (transposed in JARZEMBOWSKI 2001a). The modern predominance of the Oligoneoptera (Holometabola; Fig. 11) is not evident in the Palaeozoic fauna: (JARZEMBOWSKI &ROSS 1996). E. A. JARZEMBOWSKI 32

Fig. 9. Cumulative curve for insect mouthpart classes based on data in LABANDEIRA (in press).

Fig. 10. Provisional relationships among the major hexapod groups. Based on JARZEMBOWSKI (in press). Palaeoentomology: towards the big picture 33 Table II Insect orders and the Triassic extinction Winners (Orders originating post-Tr2)

1. Protura SILVESTRI, 1907 20. Dermaptera DE GEER, 1773 23. Isoptera BRULLÉ, 1832 ** 24. Mantodea BURMEISTER, 1838 26. Zoraptera SILVESTRI, 1913 28. Phthiraptera HAECKEL, 1896 * 32. Strepsiptera KIRBY, 1815 * 37. Hymenoptera LINNÉ, 1758 *** 39. Lepidoptera LINNÉ, 1758 41. Siphonaptera LATREILLE, 1825 * Total 10 orders * parasitic ** social *** both in part

Losers (Palaeozoic orders becoming extinct before Tr2)

5. Monura SHAROV, 1951 7. Palaeodictyoptera GOLDENBERG, 1877 8. Megasecoptera BRONGNIART, 1885 9. Diaphanopterodea HANDLIRSCH, 1919 19. Protelytroptera TILLYARD, 1931 25. Caloneurodea HANDLIRSCH, 1937 Total 6 orders

Survivors (Palaeozoic orders continuing after Tr2)

2. Collembola LUBBOCK, 1871 3. Diplura BÖRNER, 1904 4. Archaeognatha BÖRNER, 1904 ? 6. Zygentoma BÖRNER, 1904 10. Ephemeroptera HYATT &ARMS, 1890 11. Protodonata BRONGNIART, 1893! 12. Odonata FABRICIUS, 1793 13. ‘Protorthoptera’ HANDLIRSCH, 1906 ? 14. Plecoptera BURMEISTER, 1838 15. Embioptera SHIPLEY, 1904 16. Phasmatodea BRUNNER, 1893 17a. Orthoptera OLIVIER, 1789 18. Grylloblattodea BRUES &MELANDER, 1915 21. Miomoptera MARTYNOV, 1927 22. Blattodea BRUNNER, 1882 27. Psocoptera SHIPLEY, 1904 29. Thysanoptera HALIDAY, 1836 30. Hemiptera LINNÉ, 1758 31. Glosselytrodea MARTYNOV, 1938 33. Coleoptera LINNÉ, 1758 34. Raphidioptera LATREILLE, 1810 35. Megaloptera LATREILLE, 1802 36. Neuroptera LINNÉ, 1758 38. Trichoptera KIRBY, 1815 42. Mecoptera PACKARD, 1886 Total 23-25 orders

Specials

17b. Titanoptera SHAROV, 1968 (Tr only) 40. Diptera LINNÉ, 1758 (Originating during Tr extinction) Total 2 orders E. A. JARZEMBOWSKI 34

Fig. 11. Recent biodiversity of major hexapod groups (approximate).

Fig. 12. Insect orders and the Triassic extinction (left, see Table II); Phanerozoic composition (right, cf. Fig. 4).

Gigantism in fossil has been linked with high oxygen in the Carboniferous atmos- phere predicted by geophysics (DUDLEY 1998). Curiously, the true giants (e.g. protodonate insects, arthropleurid ) are actually less than one percent of all terrestrial arthropods found (per- sonal tally, southern English coalfields). Charcoal is also uncommon and less evident than in some younger non-marine insect-bearing deposits, e.g. the English Wealden. The Carboniferous giant niche seems somewhat vacant on at least a regional scale and combustion elusive as a major envi- ronmental stress. Palaeoentomology: towards the big picture 35

High level changes in Permo-Triassic insects are summarized in Fig. 12 and Table II. The dy- namics of change at the Permo-Triassic boundary are still being investigated. However, the change in hemipteran family composition, an important plant-feeding group, seems more abrupt than the changes at either the Jurassic-Cretaceous or Cretaceous- boundaries (SHCHERBAKOV 2000). Post-extinction recovery was certainly under way by the Upper Trias (ANDERSON et al. 1998; JARZEMBOWSKI &ROSS 1996). The change at the Cretaceous-Tertiary boundary is now often seen as a low taxonomic one (species level) which is hard to analyse at present in the absence of a suitable insect database (but see MITCHELL, this volume). FARRELL (1998) recognized a post- Cretaceous diversification of plant-feeding beetles (Coleoptera) after the initial radiation of the an- giospermous flowering plants. This provides independent support for coevolutionary delay (JARZEMBOWSKI &ROSS 1996). Some workers still regard the Cretaceous record as poor. This is in spite of there being 123 Cretaceous insect localities recognized, compared with 183 Tertiary ones (where the record is considered to be comparatively good) as long ago as ZHERIKHIN (1980). The localities are often of basin size!

V. CONCLUSION

There are still many challenging questions in palaeoentomology and the at the beginning of the twenty-first century. The fossil record needs to be analysed as well as de- scribed using mathematics as well as qualitative models. I have tentatively suggested that the Phanerozoic history of insects may be summarised as a logistic curve at bauplan (ordinal) level, off- set by historical contingency, notably extinction at the start of the Mesozoic. An exponential model seems more appropriate at lower (family/genus) level. This is hopefully more informative than a straight linear curve at describing Phanerozoic diversity (cf. JARZEMBOWSKI &ROSS 1996). Future work will decide the appropriateness or otherwise of such modelling. How we sample and access the fossil record still poses some special problems, not least discovering the interconnection of spe- cies which maintain ecosystems. More work is needed on the ecological implications of abiotic fac- tors like past atmospheric change.

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